Impact of Hourly Emergency Department Patient Volume on Blood Culture Contamination and Diagnostic Yield

Transcription

1 JCM Accepts, published online ahead of print on 20 March 2013 J. Clin. Microbiol. doi: /jcm Copyright 2013, American Society for Microbiology. All Rights Reserved. 1 2 Impact of Hourly Emergency Department Patient Volume on Blood Culture Contamination and Diagnostic Yield Schuyler Halverson 1, Preeti N. Malani 2,5, Duane W. Newton 3, Andrea Habicht 1, Kenneth Vander Have 1, John G. Younger 1,4 Departments of Emergency Medicine 1, Internal Medicine 2, and Pathology 3, the Biointerfaces Institute 4, University of Michigan Medical School and Veterans Affairs Ann Arbor Healthcare System, Geriatric Research Education and Clinical Center (GRECC) Corresponding Author John G Younger N North Campus Research Center 2800 Plymouth Road Ann Arbor, MI Key Words: Blood cultures, Emergency Department, Patient Safety SUMMARY: The frequency with which emergency department drawn blood cultures recovered a likely pathogen decreased and the likelihood of recovering a contaminant increased during times of high occupancy. 25 1

2 ABSTRACT Background: Emergency departments (EDs) are an important diagnostic site for outpatients with potentially serious infections. EDs frequently experience high patient volumes, and crowding has been shown to negatively impact the delivery of early care for serious infections such as pneumonia. Here we hypothesized that another important part of early care of infectious diseases, the rate of blood culture contamination and accurate detection of pathogens, would be sensitive to ED operational stress, as proper collection requires fastidious attention to technique and timing Methods: We related all blood cultures collected over one year and their rates of recovery of likely contaminants and likely pathogens to the number of patients being cared for in the ED at the time of sample collection. Likely pathogens and contaminants were classified through combined microbiological and manual chart review criteria. Zero inflated Poisson regression was used to relate crowding to culture results Results: Cultures were obtained in 7,586 patients over 82,521 adult and pediatric patient visits. The unadjusted rates of recovering a likely pathogen or contaminant were 8.0% and 3.7%, respectively. Periods of increased crowding (3 rd and 4 th quartiles of hourly occupancy) were significantly associated (p<0.01) with increased rates of contamination (relative risk 1.23 compared to least busy quartile). Cultures collected during busy times also reduced the likelihood of recovering a likely pathogen (relative risk 0.93 compared to least busy quartile) Conclusions: ED crowding was associated with degraded performance of blood culture, both increasing the rate of contamination and decreasing the diagnostic yield. 46 2

3 INTRODUCTION Despite considerable efforts to reduce their incidence, contaminated blood cultures continue to be a significant clinical problem. Ongoing multicenter monitoring in the United States places the median rate of contamination at just under 3% (lower national quartile 2.15% ; upper quartile 3.67%).(1) The clinical and financial impacts of contaminated cultures have been examined by numerous groups; the most recently published results indicate among patients undergoing blood culture during emergency department evaluation and subsequent admission to the hospital, a false positive culture adds an estimated $8,700 (2008 U.S. dollars) and an additional day of hospitalization. (5) Excess contamination rates are driven primarily by lack of operator fastidiousness during the collection process.(14) As such, interventions such as dedicated phlebotomy teams, pre packaged blood culture kits, and the use of sterile gloves have helped decrease contamination rates.(6, 15) One clinical setting about which little is known regarding blood culture contamination is the Emergency Department (ED). EDs are an important and common site for initial diagnosis and treatment, with more than 136 million visits taking place in 2009, the most recent year for which Centers for Disease Control and Prevention data are available.(13) Increasingly, EDs serve a diagnostic niche previously filled by both outpatient and inpatient venues. The expanding role of this clinical site for initial diagnosis and treatment of many urgent conditions frequently results in crowded conditions. Although typically attributed to some combination of increased utilization (i.e., more patients seeking care) or decreased availability of inpatient beds, at least one recent report indicates that growing lengths of stay for patients in EDs are a result of increasing practice intensity, a concept that includes more extensive diagnostic testing and treatment prior to ultimate patient disposition (12). Previous work demonstrates that high levels of ED occupancy may negatively impact the care and outcome of a number of time critical infectious conditions.(2, 3, 11) 3

4 Here, we propose that the rate of blood culture contamination may be an especially sensitive marker to high occupancy conditions in EDs. High visibility events such as acute myocardial infarction or stroke often prompt caregiver teams to assemble and redirect resources and attention within the ED workflow. Because the timeliness and outcome of care of these events are commonly used as performance metrics, extensive quality monitoring and improvement programs may also be present. In contrast, blood cultures may be drawn by a lone operator in relative isolation, often under time pressure to expedite the skin preparation and sampling process perhaps by using blood already drawn or preexisting vascular access sites. As blood culture results can take several days to return, and because of frequent retrospective uncertainty about the precise circumstances under which cultures are drawn, operators may receive little or no feedback to improve future performance. We therefore hypothesized that the rate of blood culture contamination in our ED would be susceptible to variation in intensity of clinical activity, which is defined here as occupancy (the total number of patients in the ED during any given time). We considered this hypothesis using operational and microbiological data from an 80,000 annual visit academic tertiary ED. 84 METHODS Emergency Department Characteristics and Determination of Activity. The University of Michigan Health System (UMHS) Emergency Department is an 80,000 annual visit facility caring for adults and children. All faculty are board certified through the American Board of Emergency Medicine and oversee fellows, residents, and physician assistants. Approximately 30% of patients seen are admitted to the hospital, and 2.6% are admitted to an intensive care unit. In our ED, blood cultures are most frequently drawn by emergency medical technicians, less frequently by nurses, and least frequently by physicians. During the study period, nurse to patient ratios in critical care areas were 2:3, and 1:4 in the remainder of the department. Technician to patient ratios were 1:9. 4

5 The number of new patient arrivals, patient length of stay (LOS) in the ED, and patient triage acuity score for each hour between October 31, 2010 and October 30, 2011 were gathered from the ED clinical information system at UMHS (Centricity 7.5.x, General Electric Healthcare, Piscataway, NJ) as we have described previously. (8, 9) Hourly occupancy was chosen over more complex crowding metrics and was reconstructed from arrival and LOS data.(7) The results of all blood cultures drawn during the study period were extracted from the UMHS Clinical Microbiology laboratory information system. Data sets from these two sources were merged using patient date of birth and ED date of service, which was possible for 99.6% of patients. All work was approved by the University of Michigan Medical School s Institutional Review Board Blood Culture Collection and Interpretation. UMHS policy for blood culture collection required initial skin preparation with one alcohol pad, followed by three iodophor swabs, ending with a one minute delay prior to venipuncture or line access. Since the reporting of blood culture source is not standardized in our institutional medical record system, identification of venipuncture versus line access was not reliable enough to be included in our analysis. We defined one set of blood cultures as one aerobic and one anaerobic bottle. All cultures were analyzed using the BacT/Alert/FAN system for detection of positive blood cultures and Vitek 2 system for identification of isolates (biomérieux, Durham, NC). The time of blood culture acquisition was assumed to be the time stamped on the blood culture requisition Cultures results were screened for contamination based on the Centers for Disease Control and Prevention / National Healthcare Safety Network definition for laboratory confirmed bloodstream infection along with Infectious Diseases clinician (P.N.M.) and microbiologist (D.N.) interpretation based on standard practice guidelines [12]. Cultures recovering diphtheroids (Corynebacterium spp not diphtheriae), Bacillus spp, Propionibacterium spp, coagulase negative staphylococci, viridans group 5

6 streptococci, Aerococcus spp, or Micrococcus spp were further investigated by manual chart review of the ED visit and associated hospitalization of the patient from whom the culture was recovered. These cultures were ultimately labeled as likely contaminant when manual chart review showed the blood culture report prompted either no additional antimicrobials, discontinuation of existing antibiotic therapy, or specific mention in the medical record that the result represented a contaminant or likely contaminant. All cultures showing bacterial growth that did not meet these criteria were deemed to have identified a likely pathogen As the primary endpoint of this study was to identify factors associated with the recovery of a contaminant organism or pathogen at the time of blood culture, it was possible for a blood culture to contain both a likely pathogen and a likely contaminant. For example, a set returning both Klebsiella pneumoniae and a diphtheroid would be considered simultaneously having returned a likely pathogen and a likely contaminant Statistical analysis. ED operational and blood culture data merge routines were written in PERL [14]. Summary statistics are presented as median and percentages, with p value <0.05 considered statistically significant. In all regression analysis, the experimental unit was the culture set, rather than the patient, as a single patient typically had multiple culture sets. We performed two sample proportion tests to compare contamination/pathogen recovery rates and Poisson regression to assess the relationship between ED activity measures and the likelihood of contamination. Preliminary analysis using Vuong s non nested hypothesis test confirmed a greater number of negative cultures than would 135 be expected from a typical Poisson distribution, so zero inflated Poisson models were used. Hourly activity measures were binned into quartiles (e.g., least busy 25% of operational hours per year). Acknowledging the uncertain delays between a blood culture actually being collected and the assignment of a time stamp for submission to the clinical laboratory, we performed analysis of risk of 6

7 contamination as a function of recorded collection time and that time lagged by one or two hours. In these analyses, a two hour lag produced a significantly improved goodness of fit as noted by minimizing the Akaike information criterion (AIC), and thus this lag was used in subsequent analysis. Statistical analysis was performed using R (R Foundation for Statistical Computing, Vienna, Austria) RESULTS During the study period, 82,521 patient encounters occurred in the UMHS ED (63,533 adults and 18,988 children). Of these, 26,695 resulted in hospitalization, with 2,136 admitted to the intensive care unit and 993 taken directly to surgery. Among all patients, 7,586 had blood cultures submitted, with a total of 12,696 distinct blood culture sets drawn in the ED. This represented 22.9% percent of the 55,476 blood culture sets processed at the entire University of Michigan Health System during the study period. In pediatric patients, single sets were drawn in 1,354 of 1,490 patients (90.0%), whereas adult patients had single sets drawn in 1,386 of 6,078 patients (22.8%). The median time between ED arrival and blood culture acquisition was 97 minutes (IQR ), a delay similar to what we have previously reported in the care of patients with sepsis in this ED. (10) The mean duration between documented time of specimen collection and delivery to the laboratory was 38 minutes (IQR 16 40). Details of patient demographics are shown in Table Among patients who had blood cultures drawn, 865 (11.4%) had at least one culture positive for bacterial growth, 606 (8.0% of total) of which grew likely pathogens while 285 (3.7% of total) were deemed likely contaminated. Note that because of our definitions, cultures recovering true pathogens and contaminants were not mutually exclusive 26 patients had cultures classified in this way. Of all individual culture sets drawn in the ED, 1188 (9.4%) were positive for bacterial growth, 913 (7.2%) of which grew true pathogens while 296 (2.3%) were deemed contaminated, giving a gross false positive 7

8 rate of 24.9%. In subset analysis of the number of sets drawn per visit, patients receiving multiple cultures were more likely to result in positive cultures (7.8%) than patients with single cultures (5.1%) (p < 0.001), although there was no difference in contamination rates (2.2% vs. 2.6% respectively, p > 0.05). When comparing the proportion of cultures recovering true pathogens or contaminants between age categories or disposition status, using age years or admission to general care as reference categories respectively, patients admitted to an ICU had an increased likelihood of recovery of a likely pathogen (p = 0.01). A total of 109 unique bacterial species were identified, with coagulase negative staphylococci, Staphylococcus aureus, and Escherichia coli recovered most frequently. Details of blood culture microbiology are shown in Table Hourly ED occupancy showed typical cyclic variation (Figure 1). Blood culture activity, including number of cultures drawn, number positive, and number contaminated, showed similar periodicity (p < versus no temporal variation) and indicated as expected that during busy times more cultures were drawn. That said, as ED occupancy increased the proportion of patients undergoing blood cultures decreased (Figure 2A, p < 0.01). There were no differences among either adult or pediatric patients in regard to the number of sets drawn per visit as a function of ED occupancy (p > 0.05 for each population, Figure 2B) Positive blood cultures, both real and contaminated, are uncommon events and thus the timing of their occurrence is not normally distributed. Therefore, we used zero inflated Poisson regression, rather than the more usual logistic regression, to relate the rate of culture contamination with the level of ED patient volume at the time of blood sampling. As ED occupancy increased, the risk of a blood culture being contaminated increased as well. When considered in a simple bivariate way, the relative risk of a positive culture returning a contaminant was 1.22 (95% CI 0.91, 1.63) in the 3 rd quartile of overall activity versus the least busy quartile, and 1.25 (95% CI 0.95, 1.60) for the 4 th quartile versus the 8

9 first. When the data were considered with the more complete zero inflated Poisson model, the relationship between ED occupancy level and contamination became even more pronounced (Figure 2C, p < 0.01). Only cultures drawn during the busiest quarter of ED operational hours were in excess of the College of American Pathologists 75 th percentile contamination rate As we had initially hypothesized, blood cultures drawn in the busiest half of all hours of the year were significantly more likely to be contaminated than those drawn in the least busy quarter. What was unexpected was that during the busiest times, the likelihood of recovering a likely pathogen decreased. Compared to the least busy quartile, the relative risk of a positive culture drawn in the 3 rd quartile of activity returning a likely pathogen was 0.94 (95% CI 0.86, 1.03). Similarly, the relative risk in the busiest quartile was 0.93 (95% CI 0.86, 1.01). As with the contamination rate, consideration of the data in the zero inflated Poisson model revealed a stronger and more statistically significant effect (Figure 2D, p < 0.01). 197 DISCUSSION In the current work, we relate ED operational activity to two markers of blood culture quality, the rate of contamination and the frequency of recovering a true pathogen. We found that both of these measures suffered during busy hours of operation. These findings suggest several important features regarding ED based blood culture testing First, the likelihood of blood culture contamination increased significantly with increased patient volume, particularly in the top 25% of busy times during the study year. Increases in the contamination rate suggest technical lapses on the part of caregivers collecting samples for culture. Prior to the conduct of this study, a widely held belief at UMHS was that the ED was disproportionately likely to contaminate blood cultures. The current results indicate that this is not true. In fact, during low occupancy times, the contamination rate in the department was commensurate with health system 9

10 wide rates and, except for the busiest times of the year, was also on par with other health systems in general as reported by the College of American Pathologists.(1) Nevertheless, the increase in contamination rate as a function of ED occupancy represents an important issue for future study and intervention. A particular question raised by our results is whether time pressure prompted an increase in drawing cultures from pre existing intravenous catheters. Our laboratory information system accommodates annotating samples as to site of collection. However, during the study period the site of collection was infrequently recorded and, when noted, was done so with ad hoc abbreviations and comments that were unreliable for formal analysis. Accordingly, it is not possible to state confidently whether samples were more likely to be drawn from existing catheters during high occupancy periods Second, although the fraction of patients from whom blood cultures were collected decreased with increasing activity in the ED, the likelihood of recovering a pathogen decreased. Given the retrospective nature of our work, we are unable to comment on the indications for testing in any particular patient or the appropriateness of testing decisions. One potential explanation is that during high occupancy times, culture bottles were incompletely filled, reducing the likelihood of recovering a pathogen. However, the observed effect of high occupancy is also consistent with a loosening of indications for blood culture during busy times. To partially address this possibility, we hypothesized that during high occupancy times, cultures would be acquired from progressively less ill patients. Using the emergency triage score as a marker for general illness severity did not reveal any differences in culture practice, although this is a very coarse metric for assessing severity of illness (data not shown) Reduced quality of blood cultures during periods of operational stress may have some role as a surrogate marker for the degradation of sterile technique in other ED processes. For example, although anecdotally a clinical location at high risk for central line associated blood stream infection (CLABSI), 10

11 data to support this claim are very sparse: in a prospective surveillance study of ED placed central venous catheters, our group was unable to substantiate increased risk. (4) However, CLABSIs are infrequent enough, and their attribution sufficiently vague, that blood cultures might serve a useful role in tracking unit clean culture more effectively and warrants further study. Additionally, that a cornerstone microbiological test was shown to be subject to operational stress may have implications for epidemic management as well, where EDs will play a central role not only in treatment but in diagnosis The primary limitation of this work is in mapping ED occupancy to the ill defined concept of crowding. At first impression, our data suggest that the appropriateness of utilization and technical acquisition of blood cultures in the ED are negatively impacted due to over extended providers, which may or may not be true. Important covariates not available to us in this analysis relate to departmental staffing details, including the number of providers actually present at any given time during the study period and reliable annotation of which type of provider collected each sample. Scheduling physicians, nurses, and technicians in a clinical environment with such strong cyclical activity is complex, as is retrospectively estimating with accuracy the number and type of providers working at any hour of the year. At our institution, retrospectively determining the presence of a non physician caregiver can only be estimated through payroll records, and in our experience these are insufficiently reliable for research use. As staffing levels for all types of providers increases during periods of high patient occupancy, it is inappropriate to conclude that our findings indicate only staffing inadequacies Similarly, attribution of a culture to a specific provider was not possible due to the lack of a consistent practice for chain of evidence type tracing of samples from the bedside to the laboratory. Establishing a more reliable means of informing individual providers of their blood culture 11

12 contamination and true positive rates would be of value in developing improved quality assurance strategies CONCLUSION The frequency with which ED blood cultures recovered a likely contaminant increased and the likelihood of recovering a pathogen decreased during times of high occupancy

13 TABLES AND FIGURES Table 1. Clinical Features of Patients Undergoing Blood Culture in the Emergency Department (ED) Patient Feature Total Patients Seen in ED Patients Cultured Likely Pathogen Recovered Likely Contaminant Recovered Age 0 60 days (3.5%) 4 (2.8%) 61 days 2.9 years 5, (9.2%) 8 (1.9%) 3 years 17.9 years 12, (5.0%) 15 (1.6%) 18 years 49 Years 36,236 2, (7.2%) 76 (3.7%) 50 years 59 years 10,691 1, (7.5%) 51 (4.0%) 60 years 69 years 7,583 1, (10.8%) 63 (5.2%) 70 years 79 years 4, (10.4%) 32 (3.8%) > 80 years 4, (7.7%) 36 (5.3%) All ages 82,521 7, (8.0%) 285 (3.8%) Disposition Hospitalized 26,695 6, (8.7%) 234 (3.8%) Admitted to general care 23,566 5, (7.7%) 187 (3.5%) Admitted to ICU 2, (14.6%)* 42 (5.8%) Transferred to OR (10.9%) 5 (5.0%) Discharged home 52,701 1, (3.3%) 17 (1.6%) Left prior to evaluation 2, (8.7%) 0 (0.0%) Died prior to discharge (37.5%) 1 (12.5%) Transfer to other facility (0.0%) 0 (0.0%) Other (12.2%) 33 (9.6%) *P < Proportions were compared to reference groups of age and admission to general care. ICU=Intensive care unit OR=operating room 13

14 Table 2. Organisms Recovered from Blood Cultures Drawn during Emergency Department Visits Likely Pathogens Frequency Staphylococcus aureus 161 Escherichia coli 152 Coagulase negative staphylococci* 124 Klebsiella pneumoniae 96 Pseudomonas aeruginosa 33 Streptococcus pneumoniae 33 Alpha hemolytic Streptococcus 32 Enterobacter cloacae 29 Streptococcus mitis 18 Klebsiella oxytoca 16 Other Species (89 total distinct species) 232 Likely Contaminants Coagulase negative staphylococci* 254 Isolates not undergoing full identification** 79 Enterococcus faecalis 47 Micrococcus species 31 Bacillus cereus 12 Vancomycin resistant E. faecium 12 Abiotrophia / Granulicatella 5 Nutritionally variant Gram Positive Coccus 5 Ochrobactrum anthropi 4 Vancomycin resistant E. faecalis 4 Enterococcus durans 2 Lactobacillus species 1 Lactococcus species 1 Microbacterium species *Designated as likely contaminant or likely pathogen based on chart review **Includes all results that were not investigated following laboratory designation of contaminant 14

15 Figure 1. Diurnal variability in emergency department (ED) blood culture activity. Bottom panel: Hourly variation in ED occupancy (the number of patients in the ED during any hour) over the week. Results reported as 5 th, 25 th, median, 75 th, and 95 th percentile values over the 1 year study period. Second from bottom panel: Number of cultures drawn per hour, using the same plotting convention. Second from top panel: Cumulative number of cultures recovering a likely pathogen during any hour of the week across the study year. Top panel: Cumulative number of cultures recovering a likely contaminant during any hour of the week across the study year. 15

16 Figure 2. Impact of hourly emergency department (ED) occupancy on culture activity and outcome. Panel A. Fraction of patients undergoing blood culture during any hour of the year as a function of hourly ED occupancy, plotted as 5 th, 25 th, 50 th, 75 th, and 95 th percentile. Panel B. Distribution of number of sets sent for each patient. Panel C. Rate of recovering a contaminant species from a blood culture. Panel D. Fraction of blood cultures recovering a pathogen

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